The adaptive genomic landscape of beak morphology in Darwin's finches.

Beak shape in Darwin's ground finches (Geospiza) is emblematic of natural selection and adaptive radiation, yet our understanding of the genetic basis of beak shape variation, and thus the genetic target of natural selection, is still evolving. Here we reveal the genomic architecture of beak shape variation using genomewide comparisons of four closely related and hybridizing species across 13 islands subject to parallel natural selection. Pairwise contrasts among species were used to identify a large number of genomic loci that are consistently related to species differences across a complex landscape. These loci are associated with hundreds of genes that have enriched GO categories significantly associated with development. One genomic region of particular interest is a section of Chromosome 1A with many candidate genes and increased linkage. The distinct, pointed beak shape of the cactus finch is linked to an excess of intermediate frequency alleles and increased heterozygosity in significant SNPs, but not across the rest of the genome. Alleles associated with pointier beaks among species were associated with pointier-beaked populations within each species, thus establishing a common basis for natural selection, species divergence and adaptive radiation. The adaptive genomic landscape for Darwin's finches mirrors theoretical expectations based on morphological variation. The implication that a large number of genes are actively maintained to facilitate beak variation across parallel populations with documented interspecies admixture challenges our understanding of evolutionary processes in the wild.

The evolutionary history of Darwin's finches: speciation, gene flow, and introgression in a fragmented landscape.

Many classic examples of adaptive radiations take place within fragmented systems such as islands or mountains, but the roles of mosaic landscapes and variable gene flow in facilitating species diversification is poorly understood. Here we combine phylogenetic and landscape genetic approaches to understand diversification in Darwin's finches, a model adaptive radiation. We combined sequence data from 14 nuclear introns, mitochondrial markers, and microsatellite variation from 51 populations of all 15 recognized species. Phylogenetic species-trees recovered seven major finch clades: ground, tree, vegetarian, Cocos Island, grey and green warbler finches, and a distinct clade of sharp-beaked ground finches (Geospiza cf. difficilis) basal to all ground and tree finches. The ground and tree finch clades lack species-level phylogenetic structure. Interisland gene flow and interspecies introgression vary geographically in predictable ways. First, several species exhibit concordant patterns of population divergence across the channel separating the Galápagos platform islands from the separate volcanic province of northern islands. Second, peripheral islands have more admixed populations while central islands maintain more distinct species boundaries. This landscape perspective highlights a likely role for isolation of peripheral populations in initial divergence, and demonstrates that peripheral populations may maintain genetic diversity through outbreeding during the initial stages of speciation.